Journal of the Mechanical Behavior of Biomedical Materials 82 (2018) 218–223 Contents lists available at ScienceDirect Journal of the Mechanical Behavior of Biomedical Materials journal homepage: www.elsevier.com/locate/jmbbm Analyzing nature's protective design: The glyptodont body armor T ⁎ Anton du Plessisa, , Chris Broeckhovenb, Igor Yadroitsevc, Ina Yadroitsavac, Stephan Gerhard le Rouxa a CT Scanner Facility, Central Analytical Facilities, Stellenbosch University, Matieland, 7602 Stellenbosch, South Africa b Laboratory of Functional Morphology, Department of Biology, University of Antwerp, Wilrijk 2610, Belgium c Department of Mechanical and Mechatronic Engineering, Central University of Technology, Bloemfontein 9300, South Africa ARTICLE INFO ABSTRACT Keywords: Many animal species evolved some form of body armor, such as scales of fish and bony plates or osteoderms of Biomimicry reptiles. Although a protective function is often taken for granted, recent studies show that body armor might Osteoderm comprise multiple functionalities and is shaped by trade-offs among these functionalities. Hence, despite the fact Micro-computed tomography that natural body armor might serve as bio-inspiration for the development of artificial protective materials, Reverse-engineering, stress simulation focussing on model systems in which body armor serves a solely protective function might be pivotal. In this study, we investigate the osteoderms of Glyptotherium arizonae, an extinct armadillo-like mammal in which body armor evolved as protection against predators and/or tail club blows of conspecifics. By using a combination of micro-computed tomography, reverse-engineering, stress simulations and mechanical testing of 3D printed models, we show that the combination of dense compact layers and porous lattice core might provide an op- timized combination of strength and high energy absorption. 1. Introduction Miocene to Pleistocene, but went extinct some 10,000 years ago. Many glyptodonts were large, up to size of a small car, and possessed a solid Various forms of protective body armor are present in the animal protective carapace consisting of interlocking osteoderms. The carapace kingdom, including the scales of fish and pangolins, the carapaces of of glyptodonts was relatively rigid, unlike the more flexible organiza- turtles and osteoderms - bony plates embedded in the skin of crocodiles tion present in armadillos (Chen et al., 2011). It has been proposed that and armadillos (Yang et al., 2012, 2013). Natural body armor comes in the armor of glyptodonts evolved either to resist attacks by large co- many shapes, ranging from overlapping, highly-flexible elements (Yang occurring predators, or more plausible, serve as protection against the et al., 2012, 2013) to rigid hexagonal structures interlocked with su- powerful tail-blows of conspecifics during intraspecific fights tures (Yang et al., 2015). The diversity in structure and associated (Alexander et al., 1999; Blanco et al., 2009; Arbour and Zanno, 2018). mechanical behavior has made natural body armor a promising can- Unlike reptiles, these mammals did not require thermal regulation, didate for the bio-inspiration of artificial protective materials (Yang eliminating this role for the dermal armor. Yet, despite its (presumably) et al., 2012, 2013; Chintapalli et al., 2014; Naleway et al., 2015; Wang sole protective function, the mechanical behavior of glyptodont osteo- et al., 2016; Torres and Lama, 2017). However, recent studies show that derms has never been investigated. natural body armor might not only fulfil a protective role, but is instead In this study, we examine the mechanical behavior of glyptodont shaped by multiple selective pressures (Broeckhoven et al., 2017). For osteoderms, with particular focus on the structural parameters that example, Broeckhoven et al. (2017) demonstrate a functional trade-off might be crucial to its protective function. To do so, we employ a between strength and thermal capacity of osteoderms in two species of combination of micro-computed tomography techniques, computer si- girdled lizards. Hence, appropriate selection of model systems for the mulation and mechanical testing, using reverse-engineered osteoderms bio-inspiration of artificial body armor, i.e. those that serve a (almost) produced by additive manufacturing. By analyzing the compressive solely protective function, is pivotal for the advancement of protective behavior and energy absorption capabilities of the glyptodont osteo- materials. derms, we aim to provide a better understanding of the configuration Glyptodonts or glyptodontines (Fig. 1) are extinct mammals be- required for carrying out a protective function, which ultimately can longing to the order Cingulata, which includes modern-day armadillos serve to improve the bio-inspiration of artificial body armor. (Delsuc et al., 2016). They roamed the American continent from the ⁎ Corresponding author. E-mail address: [email protected] (A. du Plessis). https://doi.org/10.1016/j.jmbbm.2018.03.037 Received 16 February 2018; Received in revised form 26 March 2018; Accepted 28 March 2018 Available online 29 March 2018 1751-6161/ © 2018 Elsevier Ltd. All rights reserved. A. du Plessis et al. Journal of the Mechanical Behavior of Biomedical Materials 82 (2018) 218–223 properties. This material was selected as it is particularly well suited to additive manufacturing of bio-inspired models. All simulation results were compared relative to one another only, therefore the conclusions made from these simulation results are valid for all materials in the linear elastic regime. However, in this work the testing was conducted with polymer printed models, due to limitations in the maximum compressive force of the available test equipment. Mechanical tests were conducted using a universal test machine (Model 43, MTS, 30 kN maximum force). Compression testing was performed at 1.5 mm per second. Absorption energy was calculated from the obtained stress- strain data according to the procedures in Maskery et al. (2017) and originally in Gibson and Ashby (1999). Of each different design varia- Fig. 1. Left: photograph of a fossil reconstruction of a glyptodont (here: tion, stress-strain curves were obtained for 3 replicates. Panochthus frenzelianus) showing its body armor consisting of interlocking os- teoderms. Top right: photograph of an isolated Glyptotherium arizonae osteo- 3. Results and discussion derm used in this study. Bottom right: three-dimensionally rendered micro-CT image of the isolated osteoderm showing the compact layers surrounding the 3.1. Morphological analysis and reverse engineering cancellous core. Osteoderms of Glyptotherium arizonae consist of a cancellous trabe- 2. Methods cular core sandwiched between two compact layers. Each hexagonal osteoderm is joined to the adjacent osteoderms with sutures, thereby 2.1. Micro-computed tomography and reverse engineering of osteoderms making a rigid shield or carapace, as seen in other natural body armor (Chen et al., 2011, 2015; Yang et al., 2015; Achrai and Wagner, 2017). An isolated osteoderm of Glyptotherium arizonae was purchased from A three-dimensionally rendered image of an osteoderm micro-CT scan a commercial dealer (Prehistoric Florida, Tallahassee, FL) and microCT is shown in Fig. 1. Several quantitative measurements were obtained scanned at high resolution using a GE Phoenix v|tome|x L240 dual tube from the micro-CT scan, including the thickness of the compact layer, CT instrument (Phoenix X-ray; General Electric Sensing & Technologies, the mean strut thickness of the cancellous core, and the total porosity of Wunstorf, Germany) located at the Stellenbosch micro-CT facility (Du the cancellous core. An internal rectangular region-of-interest (ROI), Plessis et al., 2016). Following the guidelines in Du Plessis et al. measuring 10 × 10 × 4 mm, was digitally extracted from the micro-CT (2017a), micro-CT scanning was conducted at 120 kV, 100 µA and with scan and was used to characterize the cancellous core in subsequent a voxel size of 30 µm. Data analysis was performed in Volume Graphics analyses (Fig. 2). Total porosity was measured using basic morpholo- VGStudioMax 3.0. Simplified reverse engineered models were created gical tools. Strut thickness measurement was performed using the based on the morphological measurements taken from micro-CT data. maximal-spheres method to find the actual thickness at every point in The models with lattice structures were created in the software Mate- the structure, thereby producing a strut thickness distribution from rialise Magics, including the lattice structure module. Models were which we obtained a mean value (Fig. 2). Total porosity of this internal produced with EOSINT P380 laser sintering system using PA2200 ROI was 66%, whereas the mean strut thickness was 0.25 mm. These polyamide powder. values, in combination with basic dimensional measurements and measurement of the total porosity of the entire osteoderm including the sides, were then used to determine parameters for a reverse-engineered 2.2. Computer simulations and mechanical testing simplified model with surrounding compact layers and lattice core. All measurements including those used for the reserve-engineered model Static load simulation was performed using a direct voxel-based are shown in Table 1. structural mechanics simulation module (see Broeckhoven et al., 2017; Our simplified reverse-engineered model consisted of a hexagonal Broeckhoven and du Plessis, 2017; Du Plessis et al., 2017b,